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In addition to stimulating crop "milk" formation in ring doves, prolactin (PRL) may promote the parental regurgitation behavior that transfers this "milk" to the young at the time of hatching. Although earlier studies suggest that previous breeding experience is an important modulator of PRL-induced parental regurgitation behavior in ring doves, the ways in which experience, hormones, and stimuli from young interact to promote parental behavior have not been well characterized in this species. In the first study, untreated, nonbreeding female doves with and without previous breeding experience were given 10 daily parental behavior tests (2 h/day) with a hungry 5- to 10-day-old foster squab. Experienced females exhibited a higher incidence of regurgitation behavior, defensive behavior, and crouching or sitting in the nest than did inexperienced females. In a second study, nonbreeding females were given 10 daily tests for parental behavior while they received sc injections of ovine PRL or vehicle. Prolactin reduced squab-directed aggression and increased the incidence of regurgitation feeding behavior of foster squabs in both experienced and inexperienced females. However, the average number of regurgitation feeding acts displayed by those PRL-treated females that showed the behavior was over eight times higher in experienced females than in inexperienced females. Previous experience also enhanced the stimulatory effects of PRL on defensive behavior and crouching or sitting in the nest. The parental behavior exhibited by nonbreeding, PRL-treated experienced females was qualitatively and quantitatively similar to that observed in normally breeding females during a single test with their own hungry 5- to 10-day-old squabs. These findings indicate that PRL and previous breeding experience both enhance the parental responsiveness of nonbreeding female doves and that under optimal hormonal, experiential, and squab exposure conditions, nonbreeding doves exhibit levels of parental activity that rival those of normally breeding parents., (Copyright 1999 Academic Press.)

The role of the preoptic area (POA) in mediating PRL-induced parental responsiveness toward young was investigated in nonbreeding-doves with previous breeding experience. Birds received microinjections of the axon-sparing excitotoxin ibotenic acid to destroy neuronal cell bodies in the POA. Sham-lesioned controls received POA injections of vehicle. Upon recovery, birds received subcutaneous injections of ovine PRL for 7 days, followed by a 2.5-hr test with a foster squab to assess parental responsiveness. Lesioned doves displayed significantly fewer parental feeding invitations, parental regurgitation feeding bouts, and total regurgitation movements than did sham-lesioned animals. As a result, nestlings given to sham-lesioned birds gained significantly more weight than those given to lesioned birds. A significant negative correlation was obtained between the extent of POA damage induced by ibotenic acid infusion and the amount of parental behavior displayed by lesioned animals. These deficits in parental behavior were apparently a selective effect of POA damage because another PRL-mediated behavior, hyperphagia, was unaffected. The results suggest that the POA is an important component of the neural circuitry underlying the expression of PRL-induced parental feeding behavior in non-breeding ring doves. Because elevated PRL levels are temporally associated with parental activity during the breeding cycle, these results also implicate the POA in the spontaneous display of parental feeding activity that occurs naturally at the time of hatching.

Prolactin stimulates the growth and development of specialized epithelial cells lining the cropsac of pigeons and doves (family Columbidae), leading to formation of "cropmilk," which is fed to the newly hatched squab. This system of milk feeding is unique among birds. To support the feeding of cropmilk, a complex array of behavioral adaptations are also supported by high levels of prolactin secretion in columbids during parenting. These specializations include elevated food intake (hyperphagia), nest attendance, and regurgitation feeding of the squab. Although prolactin is clearly important for these behavioral adaptations, the precise physiological and mechanistic bases for these behavioral effects remain controversial. The molecular mechanisms of prolactin action in the cropsac epithelium have been studied by cloning prolactin-induced genes, by cloning and expressing the pigeon prolactin receptor, and by analyzing the transcription factors that are activated after prolactin treatment. The avian (pigeon) prolactin receptor is a member of the cytokine receptor superfamily and uniquely contains a complete duplication of the extracellular ligand-binding domain. One of the early signal-transducing actions of prolactin in cropsac epithelium is the activation of signal transducer and activator of transcription (STAT) proteins via tyrosine phosphorylation. This fundamental signaling pathway is shared with mammalian prolactin target tissues. The convergent evolution of milk feeding and the behaviors that support parenting in columbids and mammals has depended on adaptation of both conserved mechanisms and divergent physiological processes.

Systemic administration of ovine prolactin (PRL) has been previously reported to stimulate parental feeding behavior toward 7-day-old foster squabs by nonbreeding ring doves with previous breeding experience. The first of the present experiments reexamined this claim in experienced, nonbreeding birds given test squabs of different ages. Each visually isolated male and female dove was given twice-daily subcutaneous injections of ovine PRL or vehicle for 7 days and then tested for parental responses toward a single 1-3, 6-8, or 11- to 13-day-old foster squab. Prolactin significantly increased the incidence or frequency of parental regurgitation-feeding episodes in tests with all three squab age groups and, in addition, increased the incidence of parental feeding invitations (squab-oriented bill openings) in tests with 6- to 8-day-old squabs. A second study explored the degree to which PRL can act directly on the central nervous system to facilitate parental activity in the absence of peripheral cues generated from PRL-induced changes in other target organs, such as those associated with crop sac growth and distension. In this experiment, 6- to 8-day-old test squabs were used to determine if parental behavior is enhanced by twice-daily intracerebroventricular (ICV) injections of PRL in doses below those required to stimulate peripheral target organs. Injection schedules and behavior testing procedures were the same as those used in Experiment 1. However, half of the ICV PRL-treated and ICV vehicle-treated birds were food deprived for 16 hr before and during the test in order to control for PRL-induced hyperphagia and resulting crop sac distension, which could confound the results by generating peripheral stimuli conductive to the display of regurgitation-feeding behavior. Intracranial injections of prolactin significantly increased the incidence of feeding behavior, parental feeding invitations, and crouching or sitting in the nest in food-deprived doves but not in freely fed animals. Empty crop sac weights of freely fed and food-deprived PRL-treated birds were not increased above control values, thus indicating that ICV PRL treatment did not result in significant stimulation of peripheral target organs. These results demonstrate a facilitative action of PRL on regurgitation-feeding responses and associated parental behaviors that is not restricted to squabs of one particular age range. They also indicate that PRL is capable of acting directly on the brain to promote these activities in the absence of PRL-induced changes in the crop sac and other peripheral target organs.

The role of prolactin in the maintenance of incubation behaviour in ring doves was re-examined and the dose-response relationships for behavioural, target tissue and body weight changes induced by injections of prolactin were compared in doves tested during the incubation phase of the breeding cycle. Doves given injections of prolactin twice a day starting on day 4 of incubation, during a 10-day period of isolation from their mates and nests, showed a higher persistence of incubation behaviour than doves injected with saline vehicle. However, the prolactin treatment failed to maintain incubation behaviour to the same extent as that observed in non-isolated untreated breeding pairs. Liver and body weights were higher and testicular weights lower in birds treated with high doses of prolactin than in non-isolated birds which had been incubating for 14 days. Good dose-response relationships were established between body, liver, crop and testes weights and the dose of prolactin administered. However, only a weak dose-response relationship was observed between prolactin and the maintenance of incubation behaviour. Overall, females injected with prolactin displayed more quiet sitting behaviour, less body weight gain and more gonadal regression than males injected with prolactin. Males in untreated breeding pairs had higher liver weights and lower crop weights than females. It is concluded that prolactin plays a role in maintaining readiness to incubate in doves, but that other factors may also contribute to this response. Further, it appears that prolactin mediates several target tissue changes which are sex-specific during incubation.

Virgin female hamsters were mated and tested once daily for maternal retrieving behavior beginning on days 0, 5, 9, 13, 15, of the 16 day gestation period to determine if responsiveness toward newborn pups changes as pregnancy proceeds. Upon initial exposure to 3 newborn pups, only a small percentage of early-to-mid-pregnant females exhibited maternal retrieving behavior spontaneously. In contrast, over half of the 15 day pregnant females displayed retrieving during the first test. Despite the high frequency of initial pup-directed aggression and cannibalism, maternal retrieval was induced in the majority of the females in all groups by repeated daily exposure to 3 newborn pups. However, no significant differences were observed in the number of pup exposure periods required to induce maternal retrieving in 0, 5, and 9 day pregnant females. It is concluded that the high level of maternal responsiveness observed in the parturient hamster develops somewhat abruptly during late pregnancy. In this respect, the pattern observed in the hamster differs from the more gradual increase in maternal responsiveness reported in mid-to-late-pregnant mice and rats.